O R I G I N A L A R T I C L E
the degree of arm elevation impacts the endurance
and cardiopulmonary adaptations of copd patients
performing upper-limb exercise: a cross-over study
Mara panEroni 1 *, carla siMonElli 1, pierantonio laVEnEZiana 2, 3,Massimiliano Gobbo 4, Manuela salEri 1, luca bianchi 1, Michele Vitacca 1
1istituti clinici Maugeri, irccs, pavia, italy; 2division of Experimental and clinical respiratory neurophysiology, sorbonne university, paris, france; 3pitié-salpêtrière charles foix hospital Group, service des Explorations fonctionnelles de la respiration, de l’Exercice et de la dyspnée (département “r3s”, pôle pragues), paris, france; 4department of physiology, university of brescia, brescia, italy
*Corresponding author: Mara Paneroni, Istituti Clinici Scientifici Maugeri, Via S. Maugeri 4, 27100 Pavia, Italy. E-mail: [email protected]
a b s t r a c t
BACKGROUND: In Chronic Obstructive Pulmonary Disease (COPD), upper limb exercise is widely recommended. However, how the degree of shoulder flexion may influence the exercise response is unknown.
aiM: We compared metabolic, ventilatory and symptomatic responses during constant-load supported and unsupported exercise performed at 80° and 120° arm elevation.
DESIGN: Randomized cross-over study.
SETTING: Pulmonary Pathophysiology Service in an Italian Respiratory Rehabilitative Division, in-patients were enrolled.
MEthods: twelve patients with moderate-to-severe copd (fEV1 51%, BMI 26.7 ± 6.3 Kg/m2) performed 4 symptom-limited constant-load tests at 70% of their individual maximal workload: 2 supported and 2 unsupported, respectively at 80° and 120° of glenohumeral joint flexion, executed in a random order.
rEsults: time to exhaustion (tlim), evaluated by Kaplan-Maier curve, was shorter at 120° than 80° arm elevation in both supported (360 vs.. 486 seconds, p=0.031) and unsupported exercise (210 vs.. 375 seconds, p=0.005). No difference in dynamic hyperinflation was found between 80° and 120° elevation, even at the peak of exercise and at iso-ventilation. When normalized to Tlim, 120° arm elevation had a significantly higher metabolic cost, heart rate, minute ventilation and dyspnea/fatigue symptoms compared to 80° elevation, both in unsupported and sup-ported conditions.
CONCLUSIONS: A larger shoulder flexion shortens per se exercise endurance due to the increased metabolic, ventilatory and cardiac response, without worsening dynamic hyperinflation.
clinical rEhabilitation iMpact: arm position should be considered when prescribing individual exercise training and may be ad-justed to modulate the workload.
(Cite this article as: paneroni M, simonelli c, laveneziana p, Gobbo M, saleri M, bianchi l, et al. the degree of arm elevation impacts the endur-ance and cardiopulmonary adaptations of COPD patients performing upper-limb exercise: a cross-over study. Eur J Phys Rehabil Med 2018;54:690-7. DOI: 10.23736/S1973-9087.18.04962-6)
Keywords: Exercise - Exercise test - Physical therapy modalities - Arm.
European Journal of Physical and Rehabilitation Medicine 2018 October;54(5):690-7 DOI: 10.23736/S1973-9087.18.04962-6 panEroni
arM ElEVation in EndurancE and cardiopulMonary adaptations of copd patiEnts European Journal of physical and rehabilitation
Medicine october 2018 Vol. 54 - No. 5
© 2018 EdiZioni MinErVa MEdica Online version at http://www.minervamedica.it
c
hronic obstructive pulmonary disease (copd) leads to dyspnea and, subsequently, to systemic dysfunc-tions such as effort intolerance and progressive decon-ditioning.1-4 furthermore, exercise in copd patients canbe strongly limited by the development of dynamic hyper-inflation (DH),5 which may be directly related to the
indi-vidual ventilatory response3, 5 or to the workload imposed
during the training program.6 in recent years, the role of
lower and upper body exercise in promoting functional in-dependence has been widely recognized as a fundamental component of rehabilitation for patients with copd with high level of evidence7, 8 however, there is little evidence
by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies (either sporadically printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other means which may allow access of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is not permitted. It is not permitted to remove, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo, or other proprietary information of the Publisher .
COPYRIGHT
©arM ElEVation in EndurancE and cardiopulMonary adaptations of copd patiEnts panEroni
Materials and methods
this is a prospective, crossover study with different inter-ventions provided in random order. We included 12 pa-tients referred at the respiratory rehabilitation division of the Istituti Clinici Scientifici Maugeri, Institute of Lu-mezzane (brescia), italy, between May 2011 and septem-ber 2012. The Ethics Committee of the Institute approved the protocol (CEC n ° 707, 18/04/2011). Signed informed consent was obtained from all participants.
this study conforms to all strobE guidelines and reports the required information accordingly (see supple-mentary Checklist).
Patients
patients who met the following criteria were eligible for the study: diagnosis of moderate-to-severe copd based on the American Thoracic Society/European Respiratory society criteria;20 clinical stability (no exacerbations or
medication change within the previous 30 days); no pre-vious participation in a pulmonary rehabilitation program within the past year. COPD diagnosis and severity level were established by means of pulmonary function tests conducted before and after administration of bronchodila-tors. Exclusion criteria were: severe comorbidities such as cardiac, orthopedic or neurological diseases; extreme dif-ficulty or inability to perform the exercise protocol; need for oxygen supplementation.
Protocol
Preliminary phase
At the first day, all patients performed two incremental tests (supported/unsupported) to define the maximal work-load they could do in supported and unsupported exercis-es. A period of 5 hours was interposed between the tests.
the incremental supported test was performed with an arm-ergometer (Rehab Trainer 881E, Monark Exercise ab, Vansbro, sweden) placed on a table in front of the seated patient. The arm crank height was adjusted so that the fulcrum of the pedals was at the level of the glenohu-meral joint (90° shoulder elevation). Before commencing the protocol, patients were familiarized with the exercise equipment (arm-ergometer). After the basal parameters had been recorded, patients performed a 1-minute unload-ed warm-up, followunload-ed by an incremental phase in which the load was increased by 5 watts at the end of each min-ute. Patients were asked to maintain the speed revolution between 50 and 60 rpm, and were encouraged to continue available on arm training, in particular concerning the most
effective intensity or the most appropriate exercise modal-ity for each patient.9-12
in pulmonary rehabilitation, many exercise modalities are used for arm training. Two main subgroups can be dis-tinguished: supported upper-limb exercise (typically ap-plied through arm cranking) and unsupported upper-limb exercise (by moving the arms without external aid).
only few physiological studies have tested different arm exercise modalities to identify which are the most ap-propriate interventions for COPD rehabilitation.13-15 they
compared the responses obtained during supported and un-supported exercise showing that both can induce dynamic hyperinflation.15
nevertheless, since unsupported training appeared to be the only modality able to improve the metabolic cost of the characteristic unsupported arm activities during daily life, this modality has been recommended as the optimal approach for arm training.6
arm training is usually performed with some degrees of shoulder flexion, which, in turn, is known to influence the ventilatory response both in healthy subjects16 and in
patients with lung disease.16, 17 baarends et al. showed that
static arm elevation, maintained for 2 minutes, can increase the metabolic and ventilatory response, especially in copd patients.18 to date, despite the fact that dynamic upper-limb
exercises are widely used in rehabilitative settings, only one study19 describes that strength exercises — performed
with the arm elevation above shoulder level — appears to be more challenging than low arm elevation exercises, but no study evaluated the influence of the degree of shoul-der elevation on patients’ performance during upper limbs endurance exercises. Moreover, as activities of the up-per limbs are often essential to maintain independence in daily life, a huge evaluation of the burden related to the tasks needs to be understood. Determining physiological responses and symptoms of different arm activities could help us to understand the mechanisms behind the difficul-ties that people with copd experience when performing upper limb activities, and could help to define how exercise training should be prescribed.
on these bases, the aim of this study was to evaluate the impact of arm elevation on the performance (time to ex-haustion) and the physiological responses of patients with moderate-to-severe copd during different constant-load, dynamic upper-limb exercises (supported vs.. unsupport-ed), being our hypothesis that higher elevation degrees may worse the exercise tolerance and high the risk of dynamic hyperinflation. by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies (either sporadically or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other means which may allow access all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is not permitted. It is not permitted to remove, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo, or other proprietary information of the Publisher .
COPYRIGHT
©panEroni arM ElEVation in EndurancE and cardiopulMonary adaptations of copd patiEnts
figure 1 shows the study design and the four experi-mental conditions. The order of the two increexperi-mental tests during the preliminary phase and of the 4 constant-load tests during the experimental phase were randomized us-ing an online dedicated software (http://www.randomiza-tion.com).
Measurements
during all tests, the measurements were carried out by means of a breath-by-breath analyzer (Vmax series 29c; Sensormedics, Milan, Italy). The tests were performed with a mouthpiece or mask, depending on the patient’s preference. Electrocardiogram (ECG) monitoring was car-ried out during the tests through a system of electrodes connected to a 6x2-lead electrocardiograph (Mortara in-struments, Milan, Italy). The peripheral oxygen satura-tion was measured by a pulse-oximeter placed on a finger (8500A; Nonin Medical, Plymouth, MN, USA. The pri-mary outcome of the study was the tlim for each test.
the variables evaluated and collected continuously dur-ing every test were the followdur-ing:
1) Ventilatory variables: minute ventilation (VE), tidal volume (Vt), respiratory rate (rr) and inspiratory capac-ity (IC). IC measurement was conducted as follows: when a stable end-expiratory volume was reached, the patients were asked to take a deep breath up to total lung capacity (TLC). To give reproducible results, a minimum of three maneuvers at the start of every test was performed. IC value was obtained by subtracting the end-expiratory lung volume to TLC.24, 25 this measure was also performed
each minute during the constant-load tests. 2) Cardiac parameter: HR.
3) Metabolic parameters: oxygen consumption (Vo2);
carbon dioxide production (Vco2); respiratory quotient
(RQ). exercising until exhaustion (due to dyspnea or fatigue). the operator stopped the test when the maximal theoretical heart rate (hr) was achieved, or if severe arrhythmias or desaturation occurred, i.e. oxygen saturation (spo2) <80%.
For the incremental unsupported test we used the Taka-hashi test: the patient was sitting on a chair holding a stick with the hands. We asked the patients to move with regular frequency (40 movements/min) the stick from the chest to a fixed level of a billboard in front of them (flexion/ extension of the elbow), starting from the knee level and raising the stick15 cm every minute. If patients reached the higher level on the billboard (level 8), patients continued the exercise at 8th level increasing the weight of the stick
(500g per minute). More details about the procedure of the test are provided elsewhere.21 the test was stopped if: 1)
the maximum theoretical HR was achieved (208bpm-0.7 X age in years);22 or 2) severe arrhythmias or severe
de-saturation (spo2<80%) occurred; or 3) patient exhaustion
(due to dyspnea or fatigue) occurred, or d) the patient was unable to perform the movement correctly.
Experimental phase
after the preliminary functional evaluation, four constant-load tests (supported/unsupported at 80/120° shoulder el-evation, respectively) within a period of 4 days were per-formed. Among each test a period of rest of at least 5 hours was taken.
supportedtest
after 1 minute of unloaded warm-up, for both 80° and 120°, we set the workload of the arm-ergometer at the equivalent of 70% of each patient’s maximal workload ob-tained during the incremental test.
unsupportedtests
Patients were asked to move the stick from the chest to a line on the billboard corresponding to 80° and 120° of flexion of the glenohumeral joint. For both conditions, after 1 min of unloaded warm-up, we loaded the stick at the equivalent of 70% of the maximal workload obtained by each patient in the incremental test and we asked the patient to maintain the effort as long as possible. For all constant-load tests, the time-to-exhaustion (tlim) was
de-fined in any of the following conditions: the maximum HR (preliminary calculated through the incremental test) was achieved; severe arrhythmias or desaturation (spo2<80%)
occurred; the patients perceived severe fatigue (borG scale for dyspnea and muscular fatigue higher than 8).23
Figure 1.—Representative images of study design.
SE: shoulder elevation; CL: constant-load; ULE: upper limb exercise. Which
tEst Who
preliminary phase day 1
WhEn Experimental phaseday 2-5
80° sE degree cl supported ulE 80° sE degree cl unsupported ulE 120° sE degree cl supported ulE
All patients underwent each test
random order random order
incremental unsupported test (Takahashi test) 90° sE incremental supported test 120° sE degree cl unsupported ulE by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies (either sporadically printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other means which may allow access of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is not permitted. It is not permitted to remove, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo, or other proprietary information of the Publisher .
COPYRIGHT
©Preliminary phase
The mean maximal workload at the end of the incremen-tal supported exercise was 38.75±10.68 watts. During the incremental unsupported test (Takahashi Test) the mean maximum weight of the stick lifted was 1.21±1.08 kg and the mean maximum level (line reached on the billboard) was 7.42±0.10.
Experimental phase
the median tlim in the constant-load tests for supported
exercise was 486 (range 330-1140) s at 80° vs. 360 (range 210-840) second at 120° (P=0.031) while for the unsup-ported exercise tlim was 375 (range 240-1200) s at 80° vs.
210 (range 120-360) s at 120° (P<0.01). Figure 2 shows the Kaplan-Meier curves for tlim for each test. A significant
4) Symptom modifications: a modified Borg scale23 from
0 (null) to 10 (maximal score) was used to assess the pa-tients’ intensity of dyspnea and rate of perceived exertion.
for the study, we analyzed the differences in the exer-cise response in different ways.
i. at the end of exercise (peak).
ii. Normalizing each variable to the time of exercise (tlim). We calculated the range of change of each variable
over tlim (in seconds) dividing the peak exercise - baseline
difference by the exercise time. This allowed us to detect changes of each variable / second.
iii. At iso-VE, i.e. at the maximum level of VE reached by each patient in each test.
Statistical analysis
data analysis was performed with a dedicated statistical software (StataCorp. LP; Stata Statistical Software: Release 12, 2011; college station, tX, usa) by a blinded researcher not involved in the study protocol. In the descriptive analy-sis, continuous variables were expressed as means±standard deviation (SD) and binary ones as percentages. A sample size of 12 subjects was calculated considering a difference in performance between 120° and 80° tests of 75±80 sec-onds, with alpha error =0.05 and beta error =0.90, accord-ing to the previous 5 tests conducted to test the feasibility of the protocol (no references in the literature were found). based on the variability of the ic measurement reported in different studies,6, 21, 24 to detect differences in the tlim
between 120° and 80° elevation in the supported and unsup-ported exercises, a descriptive analysis using Kaplan-Meier curves and Log-Rank test was conducted. To detect differ-ences in cardiorespiratory and metabolic parameters and in symptoms, we performed a non-parametric analysis using the paired-sample Wilcoxon signed-rank test. Statistical significance was considered for alpha <0.05.
Results
patients’ demographic and functional respiratory charac-teristics are shown in Table I.
Patients (N.=12) were predominantly male, elderly, with normal-weight and with a moderately decreased forced expiratory volume at 1 second (fEV1) and a severely
in-creased residual volume (RV). No abnormality in the gas exchange parameters was detected.
We performed a total of 72 tests, e.g. 2 incremental and 4 constant-load tests per patient.
table I.— Characteristics of the study patients.
Variables results Sex, M/F % 91.7/8.3 height (cm) 168±7 Weight (kg) 75±13 BMI (kg/m2) % bMi<18 % BMI > 18.5 < 25 % bMi > 25 < 30 % bMi > 30 26.7±6.3 16.67 8.33 58.33 16.67 age (years) 66±9
Drugs (number [and percentage] of subjects) • laMa • laba • inhaled corticosteroids • statins • antiplatelets • antihypertensive 11 (92%) 12 (100%) 11 (92%) 3 (25%) 4 (33%) 7 (58%) fEV1% pred 51±18 fVc % pred 85±17 fEV1/FVC 46±11 ic % pred 90±12 rV % pred 167±50 RV/TLC 0.54 ±0.09 Mip % pred 75±20 MEp % pred 83±30 6MWt (m) 504±63 pao2 (mmhg) 72±9 paco2 (mmhg) 39±2 ph 7.43±0.03 sato2% at rest 95±2
Values expressed as mean±DS unless otherwise stated.
bMi: body Mass index, laMa: long-acting antimuscarinic bronchodilators, laba: long-acting beta-adrenergic bronchodilators, fEV1: forced expiration
volume at 1st second; fVc: forced vital capacity; ic: inspiratory capacity, rV:
residual volume; Mip: maximal inspiratory pressure; MEp: maximal expiratory pressure; 6MWT: Six Minute Walk Test; PaO2: arterial oxygen pressure; paco2:
arterial co2 pressure; sato2: arterial oxygen saturation.
by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies (either or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other means which may all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is not permitted. It is not permitted block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo, or other proprietary information of
panEroni arM ElEVation in EndurancE and cardiopulMonary adaptations of copd patiEnts
Evaluation at peak of exercise
At peak exercise, no differences between 80° and 120° constant-load tests in either the supported and unsupported tests were found in Vo2, cardiac (hr), respiratory (rr,
Vt, VE) responses or in dyspnea and fatigue symptoms. an increased utilization of the anaerobic metabolic path-ways was found only in unsupported exercise at 120° with respect to 80°, where we found a higher Vco2 (10.51±3.23 vs. 8.78±2.16, P<0.05) and higher RQ (1.09±0.08 vs.
0.9766±0.07, P<0.01). IC decreased significantly during the course of the test in the 80° supported (–0.52±0.39, P<0.01) and 120° unsupported (-0.16±0.18, P<0.02) con-stant-load tests. No significant DH due to exercise was found between groups.
Analysis of each variable normalized to the time to exhaus-tion
table ii describes the differences of responses in relation to tlim. Exercising at 120° in both supported and
unsup-ported conditions produced a significant increase in re-spiratory, cardiac and fatigue responses and a major shift from aerobic to anaerobic metabolism, with respect to ex-ercising at 80° arm elevation. We find a significant differ-ence in the increase of Vo2, Vco2 and perceived dyspnea
between 120° and 80° elevation only for the unsupported exercise modality.
Analysis at iso-VE
Iso-VE, defined as the highest common level of VE reached by all patients in each test, was 20.5 L/min. At this point of VE, no significant differences were found in any variables or symptoms. IC at iso-VE did not differ decrease in tlim can be seen in both supported (P=0.046)
and unsupported exercise (P<0.01) for 120° elevation with respect to 80°.
Figure 2.—Time to exhaustion (Tlim) of CL-tests.
Above: supported upper limb exercises. Below: unsupported upper limb exercises.
80°: 80° degrees of shoulders elevation, 120°: 120° degrees of shoulders elevation.
table II.— Metabolic, cardiovascular and respiratory responses to the tests normalized to Tlim.
Variables 80° supported exercise 120° supported exercise p value 80° unsupported exercise 120° unsupported exercise p value
VE/time, mL/s 7.06 (3.35) 10.59 (5.47) 0.041 7.45 (3.76) 14.99 (5.81) <0.01
Vo2 peak/time, mL/s 1.6 (0.78) 3.26 (1.44) 0.060 1.73 (0.74) 2.612 (1.44) <0.01 Vco2 peak /time mL/s 1.79 (7.3) 2.71 (1.57) 0.060 1.57 (7.43) 3.54 (1.67) <0.01
DeltaIC/time, mL/s -0.06 (0.05) -0.04 (0.07) 0.182 -0.03 (0.08) -0.05 (0.056) 0.480
HR/time, beats/s 0.50 (0.17) 0.255 (0.1071) <0.02 0.22 (0.85) 0.33 (0.12) <0.01
Vt/time, mL/s 2.5 (1) 3.7 (1.5) 0.034 2.9 (1.37) 5.3 (1.4) <0.01
RQ/time, RQ/s 0.002 (0.002) 0.003 (0.001) 0.023 0.0024 (0.0009) 0.0051 (0.002) <0.01
RR/time, beats/s 0.63 (0.03) 0.09 (0.04) <0.02 0.07 (0.03) 0.14 (0.06) <0.01
Borg dyspnea, score/s 0.012 (0.007) 0.017 (0.011) 0.084 0.012 (0.01) 0.02 (0.01) <0.02 Borg fatigue, score/s 0.017 (0.006) 0.02 (0.008) 0.041 0.022 (0.009) 0.0413 (0.016) <0.01
Values expressed as mean±SD unless otherwise stated.
VE: minute ventilation, Vo2peak: oxygen uptake at peak of exercise; VCO2: carbon dioxide production at peak of exercise; DeltaIC: difference between basal and
postexercise inspiratory capacity; hr: heart rate; Vt: tidal volume; rQ: respiratory quotient (Vo2/VCO2); RR: respiratory rate; time: time to exhaustion.
a b 80° 80° 120° 120° 1.00 0.75 0.50 0.25 0.00 1.00 0.75 0.50 0.25 0.00
time of exercise (seconds)
time of exercise (seconds)
1000 1000 500 500 0 0 by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies (either sporadically printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other means which may allow access of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is not permitted. It is not permitted to remove, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo, or other proprietary information of the Publisher .
COPYRIGHT
©constant-load unsupported arm exercise at 80% of peak incremental exercise in copd patients and suggested that the main cause of interruption of exercise was arm fatigue and not the increase of DH. Our results, describing that arm exercise produced dh irrespective of the height of shoulder flexion, support the mentioned findings.
As regard as the influence of arm elevation on metabolic and ventilatory variables we showed that the arm elevation
per se produced an increase of the workload that seems
to be greater in unsupported than in supported exercise. also, during unsupported exercise only, we detected an increased burden of dyspnea that may be related to the more significant shift from aerobic to anaerobic metabo-lism compared to supported exercise. Our results are in line with those of dolmage et al.,28 who investigated the
effect of the maintenance of fixed supported and unsup-ported arm elevation, at rest and during leg exercise, on COPD patients. Albeit in different conditions from ours, unsupported upper limb elevation per se significantly in-creased the Vo2, Vco2, VE, rr and Vt with respect to the
control position.
possible explanations for the additional burden caused by shoulder elevation could be: 1) a different pattern of muscle activation. Data on this topic are limited, but Vel-loso et al.29 reported that some domestic activities clearly
require a higher proportion of maximal muscle effort (i.e. upper trapezius muscle) in copd patients with respect to healthy controls; 2) the loss of inspiratory force and the lesser ability to increase ventilation by neck inspiratory muscles, due to the decrease of their length. The findings by dolmage et al.,28 demonstrating that arm elevation at
rest produced a significant decrease (by 180 mL) in vital capacity, supports this suggestion; 3) the shift toward an-aerobic metabolism while maintaining arm elevation, sug-gested by the increase in Vco2 and RQ.
a possible reason for the increased anaerobic metabo-lism utilization could be related to a reduced muscle blood flow delivery to the active muscles, which reduces the lo-cal availability of oxygen and a major increase of recruit-ment of upper back stabilizing muscles that work in pro-longed isometric contraction when unsupported exercise is applied.
Clinical implications and further research
as the inclusion of arm exercise training in pulmonary re-habilitation programs is recommended,6 our results
high-light the need to consider the position of the shoulders in prescribing the exercise intensity of the arm training. Our findings also suggest that, in arm exercise training, a significantly between 120° and 80° elevation, as shown
in Figure 3. We found a difference in the time required to reach the iso-VE point in supported exercise between 80° and 120° (90.31±62.80 vs. 55.22±34.81, P<0.01). A trend to significance was detected also for unsupported ex-ercise in the difference between 80° and 120° (128 ±127
vs. 63.67±54.48, P=0.071).
Discussion
Metabolic abnormalities, abnormal gas exchange, abnor-mal lung mechanics with dynamic hyperinflation, pul-monary arterial hypertension, peripheral artery disease, heart-lung interaction and peripheral muscle dysfunctions are mainly factors limiting exercise in patients affected by COPD.26 However, this knowledge has been derived
mainly by studies performed by leg exercises and, before now, few studies have shown the pathophysiology re-sponses among different types of arm exercises. Our study helps to better describe this topic.
About the influence of arm elevation on time to exhaus-tion in 2010, colucci et al.6 showed that the performance
during upper limb endurance supported exercise shortened progressively with increasing workloads (50%, 60%, 80% of Vo2max loaded by increasing watts on the
arm-ergome-ter). Our results, in relation to their findings, suggest that the increase of shoulder elevation may be considered as a mode to increase the workload applied to arm muscles.8
this fact has been described as more evident when unsupported arm exercises which, additionally, resemble more properly the activities of daily living9 are performed.
In relation to the influence of the degree of arm eleva-tion on dh, romagnoli et al.27 investigated chest wall
kinematics by optoelectronic plethysmography during a Figure 3.—IC at iso-VE (20.5 L/min).
On the left supported upper limb exercises (P=0.2550) and on the right unsupported upper limb exercises (P=0.1167).
s: constant-load supported upper limb exercise; u: constant-load un-supported upper limb exercise; 80°: 80° degrees of shoulders elevation; 120°: 120° degrees of shoulders elevation.
80° s 120° s 4 3 2 1 4 3 2 1 ic (l iters) ic (l iters) 80° u 120° u by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies (either or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other means which may all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is not permitted. It is not permitted block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo, or other proprietary information of
panEroni arM ElEVation in EndurancE and cardiopulMonary adaptations of copd patiEnts
iting exercise intolerance due to ventilatory limitations, might lead to different results. Secondly, no evaluation was conducted on the level of muscle activation and on regional blood flow dynamics during the different exer-cise modalities. On this point, moreover, the experiments were conducted at different times of the day, with possible modifications related to circadian rhythms on many physi-ological variables such as blood flow control, perceived exertion, maximal attainable force.34
Conclusions
in moderate-to-severe copd patients, a higher level of shoulder elevation (120° vs. 80°) during upper limb endur-ance exercises, both supported and unsupported, worsens
per se the performance, elicits a more pronounced
meta-bolic, ventilatory and cardiac response and shifts the me-tabolism toward the anaerobic pathways without, however, worsening the dynamic hyperinflation. The position of the arms should thus be taken into account when defining ex-ercise training and for educational purposes when teaching patients on how to perform daily life activities optimally.
References
1. Romer LM, Polkey MI. Exercise-induced respiratory muscle fatigue: implications for performance. J Appl Physiol (1985) 2008;104:879–88. . 2. Leidy NK, Haase JE. Functional status from the patient’s perspec-tive: the challenge of preserving personal integrity. Res Nurs Health 1999;22:67–77.
3. Laviolette L, Laveneziana P; ERS Research Seminar Faculty. Dys-pnoea: a multidimensional and multidisciplinary approach. Eur Respir J 2014;43:1750–62.
4. Laveneziana P, Palange P; ERS Research Seminar Faculty. Physi-cal activity, nutritional status and systemic inflammation in COPD. Eur Respir J 2012;40:522–9.
5. Laveneziana P, Webb KA, Ora J, Wadell K, O’Donnell DE. Evolu-tion of dyspnea during exercise in chronic obstructive pulmonary dis-ease: impact of critical volume constraints. Am J Respir Crit Care Med 2011;184:1367–73.
6. colucci M, cortopassi f, porto E, castro a, colucci E, iamonti Vc, et al. Upper limb exercises using varied workloads and their as-sociation with dynamic hyperinflation in patients with COPD. Chest 2010;138:39–46.
7. ries al, bauldoff Gs, carlin bW, casaburi r, Emery cf, Mahler da,
et al. Pulmonary Rehabilitation: Joint ACCP/AACVPR Evidence-Based
Clinical Practice Guidelines. Chest 2007;131(Suppl):4S–42S.
8. castro aa, porto Ef, iamonti Vc, de souza Gf, nascimento oa, Jardim JR. Oxygen and ventilatory output during several activities of daily living performed by COPD patients stratified according to disease severity. PLoS One 2013;8:e79727.
9. Garcia-Rio F, Lores V, Mediano O, Rojo B, Hernanz A, López-Collazo E, et al. daily physical activity in patients with chronic obstructive pul-monary disease is mainly associated with dynamic hyperinflation. Am J Respir Crit Care Med 2009;180:506–12.
gradual and more functional progression of the exercise intensity could be obtained by raising the position of the arm to higher degrees of shoulder flexion, without worsen-ing the DH.
Moreover, although the evaluation of the differences be-tween unsupported and supported exercises was not within the scope of this study, the additional burden in dyspnea found only in unsupported exercise might suggest that one way to progressively increase workload in a rehabilitation program could be through the type of exercise prescribed: starting with supported exercise then increasing the effort by switching to unsupported exercise (which more opti-mally mimic ordinary tasks). Nevertheless, in this context, the risk of developing shoulder pain, tendinopathies/bur-sitis, scapular dyskinesia or other conditions would need to be carefully considered, particularly in the elderly or in patients who had previous injuries. Conversely, as activi-ties of the upper limbs are often essential to maintain inde-pendence in daily life, a reduction of the burden related to the tasks needs to be considered in some patients.30
sev-eral energy conservation techniques have been proposed and taught to patients in recent years.31, 32 dolmage et al.33
showed that, during tasks that included unsupported lifting of the upper limbs, the time to exhaustion can be increased if patients are taught to exhale while raising their arms. In the direction of energy conservation techniques, our data suggest that lowering the height of the shoulders — when performing tasks involving the upper limbs — could re-duce the workload and the metabolic cost of the task. Fur-ther studies are needed, especially in more severe copd patients.
this study enables information on arm endurance per-formance in copd with a moderate obstruction, mild respiratory muscles impairment, hyperinflation and with a quite preserved exercise tolerance. It is possible that pathophysiological exercise response (i.e. inspiratory rib cage expansion or diaphragmatic and expiratory muscle recruitment) could be different among copd with differ-ent phenotypes, with or without co-morbidities and in pa-tients with diverse obstruction severities.
Limitations of the study
Our study has some limitations. First, patients were not homogeneous with respect to the level of copd sever-ity. While all participants were classified as moderate-to-severe COPD patients, the SD value of RV%=167±50 indicates a moderate variability of resting hyperinflation. We hypothesize that stricter inclusion criteria, e.g. a de-fined cut-off of RV/TLC or including only patients
exhib-by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies (either sporadically printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other means which may allow access of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is not permitted. It is not permitted to remove, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo, or other proprietary information of the Publisher .
COPYRIGHT
©Thoracic Society, and European Respiratory Society. Ann Intern Med 2011;155:179–91.
21. Takahashi T, Jenkins SC, Strauss GR, Watson CP, Lake FR. A new unsupported upper limb exercise test for patients with chronic obstructive pulmonary disease. J Cardiopulm Rehabil 2003;23:430–7.
22. Tanaka H, Monahan KD, Seals DR. Age-predicted maximal heart rate revisited. J Am Coll Cardiol 2001;37:153–6.
23. Borg G. Perceived exertion as an indicator of somatic stress. Scand J Rehabil Med 1970;2:92–8.
24. O’Donnell DE, Revill SM, Webb KA. Dynamic hyperinflation and exercise intolerance in chronic obstructive pulmonary disease. Am J Respir Crit Care Med 2001;164:770–7.
25. Clark TJ, Freedman S, Campbell EJ, Winn RR. The ventilatory capac-ity of patients with chronic airways obstruction. Clin Sci 1969;36:307–16. 26. Vogiatzis I, Zakynthinos S. The physiological basis of rehabilitation in chronic heart and lung disease. J Appl Physiol (1985) 2013;115:16–21. 27. romagnoli i, Gigliotti f, lanini b, bruni Gi, coli c, binazzi b, et al. Chest wall kinematics and breathlessness during unsupported arm exer-cise in COPD patients. Respir Physiol Neurobiol 2011;178:242–9. 28. Dolmage TE, Maestro L, Avendano MA, Goldstein RS. The ventila-tory response to arm elevation of patients with chronic obstructive pulmo-nary disease. Chest 1993;104:1097–100.
29. Velloso M, Stella SG, Cendon S, Silva AC, Jardim JR. Metabolic and ventilatory parameters of four activities of daily living accomplished with arms in COPD patients. Chest 2003;123:1047–53.
30. Meijer K, Annegarn J, Lima Passos V, Savelberg HH, Schols AM, Wouters Ef, et al. characteristics of daily arm activities in patients with COPD. Eur Respir J 2014;43:1631–41.
31. Velloso M, Jardim JR. Functionality of patients with chronic obstruc-tive pulmonary disease: energy conservation techniques. J Bras Pneumol 2006;32:580–6.
32. silva cs, nogueira fr, porto Ef, Gazzotti Mr, nascimento oa, camelier a, et al. Dynamic hyperinflation during activities of daily living in COPD patients. Chron Respir Dis 2015;12:189–96.
33. Dolmage TE, Janaudis-Ferreira T, Hill K, Price S, Brooks D, Gold-stein RS. Arm elevation and coordinated breathing strategies in patients with COPD. Chest 2013;144:128–35.
34. Chan-Thim E, Dumont M, Moullec G, Rizk AK, Wardini R, trutschnigg b, et al. clinical impact of time of day on acute exercise response in COPD. COPD 2014;11:204–11.
10. Casaburi R, ZuWallack R. Pulmonary rehabilitation for man-agement of chronic obstructive pulmonary disease. N Engl J Med 2009;360:1329–35.
11. porto Ef, castro aa, nascimento o, oliveira rc, cardoso f, Jardim JR. Modulation of operational lung volumes with the use of salbutamol in COPD patients accomplishing upper limbs exercise tests. Respir Med 2009;103:251–7.
12. costi s, di bari M, pillastrini p, d’amico r, crisafulli E, arletti c, et al. Short-term efficacy of upper-extremity exercise training in pa-tients with chronic airway obstruction: a systematic review. Phys Ther 2009;89:443–55.
13. Martinez fJ, Vogel pd, dupont dn, stanopoulos i, Gray a, bea-mis JF. Supported arm exercise vs unsupported arm exercise in the re-habilitation of patients with severe chronic airflow obstruction. Chest 1993;103:1397–402.
14. Epstein SK, Celli BR, Martinez FJ, Couser JI, Roa J, Pollock M, et
al. arm training reduces the Vo2 and VE cost of unsupported arm
exer-cise and elevation in chronic obstructive pulmonary disease. J Cardiopulm Rehabil 1997;17:171–7.
15. Castro AA, Porto EF, Feltrim MI, Jardim JR. Asynchrony and hyper-inflation in patients with chronic obstructive pulmonary disease during two types of upper limbs exercise. Arch Bronconeumol 2013;49:241–8. 16. Couser JI Jr, Martinez FJ, Celli BR. Respiratory response and ventila-tory muscle recruitment during arm elevation in normal subjects. Chest 1992;101:336–40.
17. Epstein SK, Celli BR, Williams J, Tarpy S, Roa J, Shannon T. Ven-tilatory response to arm elevation. Its determinants and use in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 1995;152:211–6.
18. baarends EM, schols aM, slebos dJ, Mostert r, Janssen pp, Wout-ers EF. Metabolic and ventilatory response pattern to arm elevation in patients with COPD and healthy age-matched subjects. Eur Respir J 1995;8:1345–51.
19. Robles P, Araujo T, Brooks D, Zabjek K, Janaudis-Ferreira T, Mar-zolini s, et al. does limb partitioning and positioning affect acute cardio-respiratory responses during strength exercises in patients with copd? Respirology 2017;22:1336–42.
20. Qaseem a, Wilt tJ, Weinberger sE, hanania na, criner G, van der Molen t, et al.; american college of physicians; american college of chest physicians; american thoracic society; European respiratory Society. Diagnosis and management of stable chronic obstructive pul-monary disease: a clinical practice guideline update from the american college of physicians, american college of chest physicians, american
Conflicts of interest.—The authors certify that there is no conflict of interest with any financial organization regarding the material discussed in the manuscript. Authors’ contributions.—Mara paneroni: study design, analysis of data, manuscript preparation, review of manuscript; carla simonelli: manuscript
prepara-tion and review of the manuscript; pierantonio laveneziana: critical revision of manuscript for intellectual content; Massimiliano Gobbo: critical revision of manuscript for intellectual content; Manuela saleri: data collection and review of the manuscript; luca bianchi: data collection, study design and review of the manuscript; Michele Vitacca: study design, manuscript preparation, review of manuscript. All authors approved the final version of the manuscript.
Acknowledegments.—The Authors thank Laura Comini for critical revision and editing the manuscript, and Rosemary Allpress for the English revision of
the manuscript.
Article first published online: April 20, 2018. - Manuscript accepted: April 13, 2018. - Manuscript revised: March 22, 2018. - Manuscript received: August 31, 2017. by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies (either or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other means which may all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use is not permitted. It is not permitted block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, logo, or other proprietary information of
